EGFR Regulates the Development and Microarchitecture of Intratumoral Angiogenic Vasculature Capable of Sustaining Cancer Cell Intravasation

Neoplasia (United States)

Volumn 17, Issue 8, 2015, Pages 634-649

  Minder, Petra ^a   Zajac, Ewa ^a   Quigley, James P ^a   Deryugina, Elena I ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GELATINASE B; INTERLEUKIN 8; EGFR PROTEIN, HUMAN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; EXPERIMENTAL METASTASIS; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VASCULARIZATION; ANIMAL; CANCER TRANSPLANTATION; CHICK EMBRYO; CHORIOALLANTOIS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR INVASION; TUMOR MICROENVIRONMENT; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 9; MICROSCOPY, FLUORESCENCE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84963969170     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2015.08.002     Document Type: Article

References (75)

1. Burgess AW EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 2008, 26:263-274.
2. Han W, Lo HW Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcellular locations. Cancer Lett 2012, 318:124-134.
3. Ciardiello F, Tortora G EGFR antagonists in cancer treatment. N Engl J Med 2008, 358:1160-1174.
4. Wheeler DL, Dunn EF, Harari PM Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat Rev Clin Oncol 2010, 7:493-507.
5. Ohashi K, Maruvka YE, Michor F, Pao W Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J Clin Oncol 2013, 31:1070-1080.
6. Seshacharyulu P, Ponnusamy MP, Haridas D, Jain M, Ganti AK, Batra SK Targeting the EGFR signaling pathway in cancer therapy. Expert Opin Ther Targets 2012, 16:15-31.
7. Yu HA, Riely GJ Second-generation epidermal growth factor receptor tyrosine kinase inhibitors in lung cancers. J Natl Compr Canc Netw 2013, 11:161-169.
8. Lo HW EGFR-targeted therapy in malignant glioma: novel aspects and mechanisms of drug resistance. Curr Mol Pharmacol 2010, 3:37-52.
9. Pao W, Chmielecki J Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010, 10:760-774.
10. Witsch E, Sela M, Yarden Y Roles for growth factors in cancer progression. Physiology (Bethesda) 2010, 25:85-101.
11. Baba Y, Fujii M, Tokumaru Y, Kato Y Present and Future of EGFR Inhibitors for Head and Neck Squamous Cell Cancer. J Oncol 2012, 2012. [Article ID 986725, 9 pages].
12. Ou SH Second-generation irreversible epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors (TKIs): a better mousetrap? A review of the clinical evidence. Crit Rev Oncol Hematol 2012, 83:407-421.
13. Subramaniam D, He AR, Hwang J, Deeken J, Pishvaian M, Hartley ML, Marshall JL Irreversible multitargeted ErbB family inhibitors for therapy of lung and breast cancer. Curr Cancer Drug Targets 2015, 14:775-793.
14. Cripps C, Winquist E, Devries MC, Stys-Norman D, Gilbert R Epidermal growth factor receptor targeted therapy in stages III and IV head and neck cancer. Curr Oncol 2010, 17:37-48.
15. Patel SP, Kim KB, Papadopoulos NE, Hwu WJ, Hwu P, Prieto VG, Bar-Eli M, Zigler M, Dobroff A, Bronstein Y, et al. A phase II study of gefitinib in patients with metastatic melanoma. Melanoma Res 2011, 21:357-363.
16. Chong CR, Janne PA The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 2013, 19:1389-1400.
17. Wakeling AE, Guy SP, Woodburn JR, Ashton SE, Curry BJ, Barker AJ, Gibson KH ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 2002, 62:5749-5754.
18. Yan Y, Lu Y, Wang M, Vikis H, Yao R, Wang Y, Lubet RA, You M Effect of an epidermal growth factor receptor inhibitor in mouse models of lung cancer. Mol Cancer Res 2006, 4:971-981.
19. Friess T, Scheuer W, Hasmann M Erlotinib antitumor activity in non-small cell lung cancer models is independent of HER1 and HER2 overexpression. Anticancer Res 2006, 26:3505-3512.
20. Li D, Ambrogio L, Shimamura T, Kubo S, Takahashi M, Chirieac LR, Padera RF, Shapiro GI, Baum A, Himmelsbach F, et al. BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene 2008, 27:4702-4711.
21. Zhang D, LaFortune TA, Krishnamurthy S, Esteva FJ, Cristofanilli M, Liu P, Lucci A, Singh B, Hung MC, Hortobagyi GN, et al. Epidermal growth factor receptor tyrosine kinase inhibitor reverses mesenchymal to epithelial phenotype and inhibits metastasis in inflammatory breast cancer. Clin Cancer Res 2009, 15:6639-6648.
22. Zhou W, Ercan D, Chen L, Yun CH, Li D, Capelletti M, Cortot AB, Chirieac L, Iacob RE, Padera R, et al. Novel mutant-selective EGFR kinase inhibitors against EGFR T790M. Nature 2009, 462:1070-1074.
23. Furugaki K, Moriya Y, Iwai T, Yorozu K, Yanagisawa M, Kondoh K, Fujimoto-Ohuchi K, Mori K Erlotinib inhibits osteolytic bone invasion of human non-small-cell lung cancer cell line NCI-H292. Clin Exp Metastasis 2011, 28:649-659.
24. Ferrara N, Gerber HP, LeCouter J The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
25. Goel HL, Mercurio AM VEGF targets the tumour cell. Nat Rev Cancer 2013, 13:871-882.
26. Kobayashi Y Neutrophil infiltration and chemokines. Crit Rev Immunol 2006, 26:307-316.
27. Waugh DJ, Wilson C The interleukin-8 pathway in cancer. Clin Cancer Res 2008, 14:6735-6741.
28. Tazzyman S, Lewis CE, Murdoch C Neutrophils: key mediators of tumour angiogenesis. Int J Exp Pathol 2009, 90:222-231.
29. Gregory AD, McGarry Houghton A Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 2011, 71:2411-2416.
30. Piccard H, Muschel RJ, Opdenakker G On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit Rev Oncol Hematol 2012, 82:296-309.
31. Galdiero MR, Garlanda C, Jaillon S, Marone G, Mantovani A Tumor associated macrophages and neutrophils in tumor progression. J Cell Physiol 2013, 228:1404-1412.
32. Tazzyman S, Niaz H, Murdoch C Neutrophil-mediated tumour angiogenesis: subversion of immune responses to promote tumour growth. Semin Cancer Biol 2013, 23:149-158.
33. Elpek KG, Cremasco V, Shen H, Harvey CJ, Wucherpfennig KW, Goldstein DR, Monach PA, Turley SJ The tumor microenvironment shapes lineage, transcriptional, and functional diversity of infiltrating myeloid cells. Cancer Immunol Res 2014, 2:655-667.
34. Deryugina EI, Zijlstra A, Partridge JJ, Kupriyanova TA, Madsen MA, Papagiannakopoulos T, Quigley JP Unexpected effect of matrix metalloproteinase down-regulation on vascular intravasation and metastasis of human fibrosarcoma cells selected in vivo for high rates of dissemination. Cancer Res 2005, 65:10959-10969.
35. Partridge JJ, Madsen MA, Ardi VC, Papagiannakopoulos T, Kupriyanova TA, Quigley JP, Deryugina EI Functional analysis of matrix metalloproteinases and tissue inhibitors of metalloproteinases differentially expressed by variants of human HT-1080 fibrosarcoma exhibiting high and low levels of intravasation and metastasis. J Biol Chem 2007, 282:35964-35977.
36. Conn EM, Botkjaer KA, Kupriyanova TA, Andreasen PA, Deryugina EI, Quigley JP Comparative analysis of metastasis variants derived from human prostate carcinoma cells: roles in intravasation of VEGF-mediated angiogenesis and uPA-mediated invasion. Am J Pathol 2009, 175:1638-1652.
37. Juncker-Jensen A, Deryugina EI, Rimann I, Zajac E, Kupriyanova TA, Engelholm LH, Quigley JP Tumor MMP-1 activates endothelial PAR1 to facilitate vascular intravasation and metastatic dissemination. Cancer Res 2013, 73:4196-4211.
38. Deryugina, E. Chorioallantoic membrane microtumor model to study the mechanisms of tumor angiogenesis, vascular permeability and tumor cell intravasation. In: Angiogenesis Protocols, Third Edition. Eds. Martin SG, Hewett P. (in press).
39. Zajac E, Schweighofer B, Kupriyanova TA, Juncker-Jensen A, Minder P, Quigley JP, Deryugina EI Angiogenic capacity of M1- and M2-polarized macrophages is determined by the levels of TIMP-1 complexed with their secreted proMMP-9. Blood 2013, 122:4054-4067.
40. Ossowski L, Reich E Experimental model for quantitative study of metastasis. Cancer Res 1980, 40:2300-2309.
41. Muller PY, Janovjak H, Miserez AR, Dobbie Z Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 2002, 32. 1372-1374, 1376, 1378-1379.
42. Livak KJ, Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
43. Kim J, Yu W, Kovalski K, Ossowski L Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 1998, 94:353-362.
44. Zijlstra A, Seandel M, Kupriyanova TA, Partridge JJ, Madsen MA, Hahn-Dantona EA, Quigley JP, Deryugina EI Proangiogenic role of neutrophil-like inflammatory heterophils during neovascularization induced by growth factors and human tumor cells. Blood 2006, 107:317-327.
45. Bekes EM, Schweighofer B, Kupriyanova TA, Zajac E, Ardi VC, Quigley JP, Deryugina EI Tumor-recruited neutrophils and neutrophil TIMP-free MMP-9 regulate coordinately the levels of tumor angiogenesis and efficiency of malignant cell intravasation. Am J Pathol 2011, 179:1455-1470.
46. Bekes EM, Deryugina EI, Kupriyanova TA, Zajac E, Botkjaer KA, Andreasen PA, Quigley JP Activation of pro-uPA is critical for initial escape from the primary tumor and hematogenous dissemination of human carcinoma cells. Neoplasia 2011, 13:806-821.
47. Deryugina EI, Zajac E, Juncker-Jensen A, Kupriyanova TA, Welter L, Quigley JP Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing mmp-9 in the tumor microenvironment. Neoplasia 2014, 16:771-788.
48. Zijlstra A, Mellor R, Panzarella G, Aimes RT, Hooper JD, Marchenko ND, Quigley JP A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 2002, 62:7083-7092.
49. Tabernero J The role of VEGF and EGFR inhibition: implications for combining anti-VEGF and anti-EGFR agents. Mol Cancer Res 2007, 5:203-220.
50. Nozawa H, Chiu C, Hanahan D Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 2006, 103:12493-12498.
51. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000, 2:737-744.
52. Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci U S A 2007, 104:20262-20267.
53. Chinnaiyan P, Harari PM Clinical advancement of EGFR inhibitors in cancer therapy. Methods Mol Biol 2006, 327:189-202.
54. Wong KK Searching for a magic bullet in NSCLC: the role of epidermal growth factor receptor mutations and tyrosine kinase inhibitors. Lung Cancer 2008, 60(Suppl 2):S10-S18.
55. Ren W, Korchin B, Zhu QS, Wei C, Dicker A, Heymach J, Lazar A, Pollock RE, Lev D Epidermal growth factor receptor blockade in combination with conventional chemotherapy inhibits soft tissue sarcoma cell growth in vitro and in vivo. Clin Cancer Res 2008, 14:2785-2795.
56. Xue C, Wyckoff J, Liang F, Sidani M, Violini S, Tsai KL, Zhang ZY, Sahai E, Condeelis J, Segall JE Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis. Cancer Res 2006, 66:192-197.
57. Kedrin D, Wyckoff J, Boimel PJ, Coniglio SJ, Hynes NE, Arteaga CL, Segall JE ERBB1 and ERBB2 have distinct functions in tumor cell invasion and intravasation. Clin Cancer Res 2009, 15:3733-3739.
58. Dong Y, He Y, de Boer L, Stack MS, Lumley JW, Clements JA, Hooper JD The cell surface glycoprotein CUB domain-containing protein 1 (CDCP1) contributes to epidermal growth factor receptor-mediated cell migration. J Biol Chem 2012, 287:9792-9803.
59. Zhou ZN, Sharma VP, Beaty BT, Roh-Johnson M, Peterson EA, Van Rooijen N, Kenny PA, Wiley HS, Condeelis JS, Segall JE Autocrine HBEGF expression promotes breast cancer intravasation, metastasis and macrophage-independent invasion in vivo. Oncogene 2014, 33:3784-3793.
60. Cerniglia GJ, Pore N, Tsai JH, Schultz S, Mick R, Choe R, Xing X, Durduran T, Yodh AG, Evans SM, et al. Epidermal growth factor receptor inhibition modulates the microenvironment by vascular normalization to improve chemotherapy and radiotherapy efficacy. PLoS One 2009, 4. 10.1371/journal.pone.0006539.
61. Hirata A, Ogawa S, Kometani T, Kuwano T, Naito S, Kuwano M, Ono M ZD1839 (Iressa) induces antiangiogenic effects through inhibition of epidermal growth factor receptor tyrosine kinase. Cancer Res 2002, 62:2554-2560.
62. Ellis LM Epidermal growth factor receptor in tumor angiogenesis. Hematol Oncol Clin North Am 2004, 18:1007-1021. [viii].
63. De Luca A, Carotenuto A, Rachiglio A, Gallo M, Maiello MR, Aldinucci D, Pinto A, Normanno N The role of the EGFR signaling in tumor microenvironment. J Cell Physiol 2008, 214:559-567.
64. Dvorak HF Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 2002, 20:4368-4380.
65. Haqqani AS, Sandhu JK, Birnboim HC Expression of interleukin-8 promotes neutrophil infiltration and genetic instability in mutatect tumors. Neoplasia 2000, 2:561-568.
66. De Larco JE, Wuertz BR, Furcht LT The potential role of neutrophils in promoting the metastatic phenotype of tumors releasing interleukin-8. Clin Cancer Res 2004, 10:4895-4900.
67. Greenberg JI, Shields DJ, Barillas SG, Acevedo LM, Murphy E, Huang J, Scheppke L, Stockmann C, Johnson RS, Angle N, et al. A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 2008, 456:809-813.
68. Weis SM, Cheresh DA Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 2011, 17:1359-1370.
69. Argiris A, Kotsakis AP, Hoang T, Worden FP, Savvides P, Gibson MK, Gyanchandani R, Blumenschein GR, Chen HX, Grandis JR, et al. Cetuximab and bevacizumab: preclinical data and phase II trial in recurrent or metastatic squamous cell carcinoma of the head and neck. Ann Oncol 2013, 24:220-225.
70. Falchook GS, Naing A, Wheler JJ, Tsimberidou AM, Zinner R, Hong DS, Fu S, Piha-Paul SA, Janku F, Hess KR, et al. Dual EGFR inhibition in combination with anti-VEGF treatment in colorectal cancer. Oncoscience 2014, 1:540-549.
71. Moehler M, Thomaidis T, Zeifri C, Barhoom T, Marquardt J, Ploch P, Schattenberg J, Maderer A, Schimanski CC, Weinmann A, et al. Inclusion of targeted therapies in the standard of care for metastatic colorectal cancer patients in a German cancer center: the more the better?!. J Cancer Res Clin Oncol 2015, 141:515-522.
72. Quigley JP, Deryugina EI Combating angiogenesis early: Potential of targeting tumor-recruited neutrophils in cancer therapy. Future Oncol 2012, 8:5-8.
73. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109:625-637.
74. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
75. Farina AR, Mackay AR Gelatinase B/MMP-9 in Tumour Pathogenesis and Progression. Cancers (Basel) 2014, 6:240-296.